Effect of a tapasin mutant on the assembly of the mouse MHC class i molecule H2-Kd

Immunology and Cell Biology

Volumn 88, Issue 1, 2010, Pages 57-62

  Simone, Laura C ^a   Wang, Xiaojian ^a   Tuli, Amit ^a,b   Solheim, Joyce C ^a,b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Antigen presentation; Cysteine; ERp57; H2 Kd; Major histocompatibility complex; Tapasin

Indexed keywords

CYSTEINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MUTANT PROTEIN; PROTEIN P57; TAPASIN; CARRIER PROTEIN; DISULFIDE; H2 ANTIGEN; PDIA3 PROTEIN, MOUSE; PROTEIN DISULFIDE ISOMERASE;

AMINO ACID ANALYSIS; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; COVALENT BOND; H2 SYSTEM; HEAVY CHAIN; HUMAN; HUMAN CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULE; MOUSE; MUTATION; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; ANIMAL; CELL LINE; GENETICS; IMMUNOLOGY; METABOLISM; PROTEIN BINDING;

ANIMALS; CELL LINE; DISULFIDES; H-2 ANTIGENS; HUMANS; MEMBRANE TRANSPORT PROTEINS; MICE; MUTATION; PROTEIN BINDING; PROTEIN DISULFIDE-ISOMERASES;

EID: 74249106518     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2009.59     Document Type: Article

References (51)

1. Pamer E, Cresswell P. Mechanisms of MHC class I-restricted antigen processing. Annu Rev Immunol 1998; 16: 323-358.
2. Paquet ME, Cohen-Doyle M, Shore GC, Williams DB. Bap29/31 influences the intracellular traffic of MHC class I molecules. J Immunol 2004; 172: 7548-7555.
3. Park B, Lee S, Kim E, Cho K, Riddell SR, Cho S et al. Redox regulation facilitates optimal peptide selection by MHC class I during antigen processing. Cell 2006; 127: 369-382.
4. Farmery MR, Allen S, Allen AJ, Bulleid NJ. The role of ERp57 in disulfide bond formation during the assembly of major histocompatibility complex class I in a synchronized semipermeabilized cell translation system. J Biol Chem 2000; 275: 14933-14938.
5. Ortmann B, Copeman J, Lehner PJ, Sadasivan B, Herberg JA, Grandea AG et al. A critical role for tapasin in the assembly and function of multimeric MHC class I-TAP complexes. Science 1997; 277: 1306-1309.
6. Grandea III AG, Golovina TN, Hamilton SE, Sriram V, Spies T, Brutkiewicz RR et al. Impaired assembly yet normal trafficking of MHC class I molecules in tapasin mutant mice. Immunity 2000; 13: 213-222.
7. Garbi N, Tan P, Diehl AD, Chambers BJ, Ljunggren H-G, Momburg F et al. Impaired immune responses and altered peptide repertoire in tapasin-deficient mice. Nature Immunol 2000; 3: 234-238.
8. Sadasivan B, Lehner PJ, Ortmann B, Spies T, Cresswell P. Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP. Immunity 1996; 5: 103-114.
9. Grandea III AG, Androlewicz MJ, Athwal RS, Geraghty DE, Spies T. Dependence of peptide binding by MHC class I molecules on their interaction with TAP. Science 1995; 270: 105-108.
10. Copeman J, Bangia N, Cross JC, Cresswell P. Elucidation of the genetic basis of the antigen presentation defects in the mutant cell line .220 reveals polymorphism and alternative splicing of the tapasin gene. Eur J Immunol 1998; 28: 3788-3791.
11. Li S, Paulsson KM, Chen S, Sjögren H-O, Wang P. Tapasin is required for efficient peptide binding to transporter associated with antigen processing. J Biol Chem 2000; 275: 1581-1586.
12. Solheim JC, Harris MR, Kindle CS, Hansen TH. Prominence of b2-microglobulin, class I heavy chain conformation, and tapasin in the interactions of class I heavy chain with calreticulin and the transporter associated with antigen processing. J Immunol 1997; 158: 2236-2241.
13. Lehner PJ, Surman MJ, Cresswell P. Soluble tapasin restores MHC class I expression and function in the tapasin-negative cell line .220. Immunity 1998; 8: 221-231.
14. Bangia N, Lehner PJ, Hughes EA, Surman M, Cresswell P. The N-terminal region of tapasin is required to stabilize the MHC class I loading complex. Eur J Immunol 1999; 29: 1858-1870.
15. Li S, Sjögren H-O, Hellman U, Pettersson RF, Wang P. Cloning and functional characterization of a subunit of the transporter associated with antigen processing. Proc Natl Acad Sci USA 1997; 94: 8708-8713.
16. Li S, Paulsson KM, Sjogren H-O, Wang P. Peptide-bound major histocompatibility complex class I molecules associate with tapasin before dissociation from transporter associated with antigen processing. J Biol Chem 1999; 274: 8649-8654.
17. Grandea III AG, Comber PG, Wenderfer SE, Schoenhals G, Fruh K, Monaco JJ et al. Sequence, linkage to H2-K, and function of mouse tapasin in MHC class I assembly. Immunogenetics 1998; 48: 260-265.
18. Deverson EV, Powis SJ, Morrice NA, Herberg JA, Trowsdale J, Butcher GW. Rat tapasin: cDNA cloning and identification as a component of the class I MHC assembly complex. Genes Immun 2001; 2: 48-51.
19. Tan P, Kropshofer H, Mandelboim O, Bulbuc N, Hämmerling GJ, Momburg F. Recruitment of MHC class I molecules by tapasin into the transporter associated with antigen processing-associated complex is essential for optimal peptide loading. J Immunol 2002; 168: 1950-1960.
20. Petersen JL, Hickman-Miller HD, McIlhaney MM, Vargas SE, Purcell AW, Hildebrand WH et al. A charged amino acid residue in the transmembrane/ cytoplasmic region of tapasin influences MHC class I assembly and maturation. J Immunol 2005; 174: 962-969.
21. Dick TP, Bangia N, Peaper DR, Cresswell P. Disulfide bond isomerization and the assembly of MHC class I-peptide complexes. Immunity 2002; 16: 87-98.
22. Dong G, Wearsch PA, Peaper DR, Cresswell P, Reinisch KM. Insights into MHC class I peptide loading from the structure of the tapasin-ERp57 thiol oxidoreductase heterodimer. Immunity 2009; 30: 21-32.
23. Peaper DR, Wearsch PA, Cresswell P. Tapasin and ERp57 form a stable disulfide-linked dimer within the MHC class I peptide-loading complex. EMBO J 2005; 24: 3613-3623.
24. Garbi N, Hammerling G, Tanaka S. Interaction of ERp57 and tapasin in the generation of MHC class I-peptide complexes. Curr Opin Immunol 2007; 19: 1-7.
25. Antoniou AN, Powis SJ. Characterization of the ERp57-Tapasin complex by rapid cellular acidification and thiol modification. Antioxid Redox Signal 2003; 5: 375-379.
26. Kienast A, Preuss M, Winkler M, Dick TP. Redox regulation of peptide receptivity of major histocompatibility complex class I molecules by ERp57 and tapasin. Nat Immunol 2007; 8: 864-872.
27. Santos SG, Campbell EC, Lynch S, Wong V, Antoniou AN, Powis SJ. Major histocompatibility complex class I-ERp57-tapasin interactions within the peptide-loading complex. J Biol Chem 2007; 282: 17587-17593.
28. Chambers JE, Jessop CE, Bulleid NJ. Formation of a major histocompatibility complex class I tapasin disulfide indicates a change in spatial organization of the peptideloading complex during assembly. J Biol Chem 2008; 283: 1862-1869.
29. Rizvi SM, Raghavan M. Direct peptide-regulatable interactions between MHC class I molecules and tapasin. Proc Natl Acad Sci USA 2006; 103: 18220-18225.
30. Chen M, Bouvier M. Analysis of interactions in a tapasin/class I complex provides a mechanism for peptide selection. EMBO J 2007; 26: 1681-1690.
31. Wearsch PA, Cresswell P. Selective loading of high-affinity peptides onto major histocompatibility complex class I molecules by the tapasin-ERp57 heterodimer. Nat Immunol 2007; 8: 873-881.
32. Krangel MS, Orr HT, Strominger JL. Assembly and maturation of HLA-A and HLA-B antigens. Cell 1979; 18: 979-991.
33. Owen MJ, Kissonerghis A-M, Lodish HF. Biosynthesis of HLA-A and HLA-B antigens in vivo. J Biol Chem 1980; 255: 9678-9684.
34. Yewdell JW, Bennink JR. Brefeldin A specifically inhibits presentation of protein antigens to cytotoxic T lymphocytes. Science 1989; 244: 1072-1075.
35. Doms RW, Russ G, Yewdell JW. Brefeldin A redistributes resident and itinerant Golgi proteins to the endoplasmic reticulum. J Cell Biol 1989; 109: 61-72.
36. Watts S, Wheeler C, Morse R, Goodenow RS. Amino acid comparison of the class I antigens of the mouse major histocompatibility complex. Immunogenetics 1989; 30: 390-392.
37. Peaper DR, Cresswell P. The redox activity of ERp57 is not essential for its functions in MHC class I peptide loading. Proc Natl Acad Sci USA 2008; 105: 10477-10482.
38. Myers NB, Harris MR, Connolly JM, Lybarger L, Yu YY, Hansen TH. Kb, Kd, and Ld molecules share common tapasin dependencies as determined using a novel epitope tag. J Immunol 2000; 165: 5656-5663.
39. Simone LC, Wang X, Tuli A, McIlhaney MM, Solheim JC. Influence of the tapasin C-terminus on the assembly of MHC class I allotypes. Immunogenetics 2009; 61: 43-54.
40. Zernich D, Purcell AW, Macdonald WA, Kjer-Nielsen L, Ely LK, Laham N et al. Natural HLA class I polymorphism controls the pathway of antigen presentation and susceptibility to viral evasion. J Exp Med 2004; 200: 13-24.
41. Garbi N, Tanaka S, Momburg F, Hammerling GJ. Impaired assembly of the major histocompatibility complex class I peptide-loading complex in mice deficient in the oxidoreductase ERp57. Nat Immunol 2006; 7: 93-102.
42. Howarth M, Williams A, Tolstrup AB, Elliot T. Tapasin enhances MHC class I peptide presentation according to peptide half-life. Proc Natl Acad Sci USA 2004; 101: 11737-11742.
43. Yu YYL, Myers NB, Hilbert CH, Harris MR, Balendiran GK, Hansen TH. Definition and transfer of a serological epitope specific for peptide-empty forms of MHC class I. Int Immunol 1999; 11: 1897-1906.
44. Harris MR, Lybarger L, Myers NB, Hilbert C, Solheim JC, Hansen TH et al. Interactions of HLA-B27 with the peptide loading complex as revealed by heavy chain mutations. Int Immunol 2001; 13: 1275-1282.
45. Lybarger L, Yu YYL, Chun T, Wang C-R, Grandea III AG, Van Kaer L et al. Tapasin enhances peptide-induced expression of H2-M3 molecules, but is not required for the retention of open conformers. J Immunol 2001; 167: 2097-2105.
46. Solheim JC, Carreno BM, Smith JD, Gorka J, Myers NB, Wen Z et al. Binding of peptides lacking consensus anchor residue alters H-2Ld serologic recognition. J Immunol 1993; 151: 5387-5397.
47. Smith JD, Myers NB, Gorka J, Hansen TH. Model for the in vivo assembly of nascent Ld class I molecules and for the expression of unfolded Ld molecules at the cell surface. J Exp Med 1993; 178: 2035-2046.
48. Ozato K, Evans GA, Shykind B, Margulies D, Seidman JG. Hybrid H-2 histocompatibility gene products assign domains recognized by alloreactive T cells. Proc Natl Acad Sci USA 1983; 80: 2040-2043.
49. Nieto MC, Song ES, McKinney D, McMillan M, Goodenow RS. The association of H-2Ld with human b-2 microglobulin induces localized conformational changes in the a-1 and -2 superdomain. Immunogenetics 1989; 30: 361-369.
50. Solheim JC, Carreno BM, Myers NB, Lee DR, Hansen TH. Peptide-induced rescue of serologic epitopes on class I MHC molecules. J Immunol 1995; 154: 1188-1197.
51. Harris MR, Lybarger L, Yu YYL, Myers NB, Hansen TH. Association of ERp57 with mouse MHC class I molecules is tapasin dependent and mimics that of calreticulin and not calnexin. J Immunol 2001; 166: 6686-6692.